The role of extracellular vesicles: An epigenetic view of the cancer microenvironment

BioMed Research International

Volumn 2015, Issue , 2015, Pages

  Qian, Zhongrun ^a   Shen, Qi ^b   Yang, Xi ^a   Qiu, Yongming ^a   Zhang, Wenbin ^c  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; NUCLEIC ACID; PROTEIN; UNTRANSLATED RNA; TUMOR MARKER;

CANCER DIAGNOSIS; CANCER PATIENT; CANCER PROGNOSIS; CARCINOGENESIS; CELL FUNCTION; CELL PROLIFERATION; CHROMATIN STRUCTURE; DEMETHYLATION; DNA METHYLATION; DNA MODIFICATION; EPIGENETICS; EXOSOME; GENE ACTIVATION; GENE CONTROL; GENE INACTIVATION; HISTONE MODIFICATION; HUMAN; IMMUNOCOMPETENT CELL; METASTASIS; NEOPLASM; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW; TUMOR MICROENVIRONMENT; TUMOR SUPPRESSOR GENE; CELL COMMUNICATION; CELL TRANSFORMATION; GENETIC EPIGENESIS; GENETICS; PATHOLOGY;

BIOMARKERS, TUMOR; CELL COMMUNICATION; CELL TRANSFORMATION, NEOPLASTIC; EPIGENESIS, GENETIC; EXOSOMES; EXTRACELLULAR VESICLES; HUMANS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84947581097     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2015/649161     Document Type: Review

References (94)

1. E. J. van der Vlist, E. N. M. Nolte-'t Hoen, W. Stoorvogel, G. J. A. Arkesteijn, and M. H. M. Wauben, "Fluorescent labeling of nano-sized vesicles released by cells and subsequent quantitative and qualitative analysis by high-resolution fow cytometry," Nature Protocols, vol. 7, no. 7, pp. 1311-1326, 2012.
2. G. Raposo and W. Stoorvogel, "Extracellular vesicles: exosomes, microvesicles, and friends," The Journal of Cell Biology, vol. 200, no. 4, pp. 373-383, 2013.
3. A. V. G. de Andrade, G. Bertolino, J. Riewaldt et al., "Extracellular vesicles secreted by bone marrow-and adipose tissue-derived mesenchymal stromal cells fail to suppress lymphocyte proliferation," Stem Cells and Development, vol. 24, no. 11, pp. 1374-1376, 2015.
4. B. Mytar, M. Baj-Krzyworzeka, M. Majka, D. Stankiewicz, and M. Zembala, "Human monocytes both enhance and inhibit the growth of human pancreatic cancer in SCID mice," Anticancer Research, vol. 28, no. 1, pp. 187-192, 2008.
5. J. Ratajczak, K. Miekus, M. Kucia et al., "Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery," Leukemia, vol. 20, no. 5, pp. 847-856, 2006.
6. H. K. Kim, K. S. Song, Y. S. Park et al., "Elevated levels of circulating platelet microparticles, VEGF, IL-6 and RANTES in patients with gastric cancer: possible role of a metastasis predictor," European Journal of Cancer, vol. 39, no. 2, pp. 184-191, 2003.
7. O. Rechavi, I. Goldstein, and Y. Kloog, "Intercellular exchange of proteins: the immune cell habit of sharing," FEBS Letters, vol. 583, no. 11, pp. 1792-1799, 2009.
8. S. D'Agostino, M. Salamone, I. Di Liegro, and M. L. Vittorelli, "Membrane vesicles shed by oligodendroglioma cells induce neuronal apoptosis," International Journal of Oncology, vol. 29, no. 5, pp. 1075-1085, 2006.
9. M. C. Deregibus, V. Cantaluppi, R. Calogero et al., "Endothelial progenitor cell-derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA," Blood, vol. 110, no. 7, pp. 2440-2448, 2007.
10. J. Skog, T. Würdinger, S. van Rijn et al., "Glioblastoma micro-vesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers," Nature Cell Biology, vol. 10, no. 12, pp. 1470-1476, 2008.
11. A. Bobrie, M. Colombo, G. Raposo, and C. Téry, "Exo-some secretion: molecular mechanisms and roles in immune responses," Tra f c, vol. 12, no. 12, pp. 1659-1668, 2011.
12. S. Mathivanan, H. Ji, and R. J. Simpson, "Exosomes: extracellular organelles important in intercellular communication," Journal of Proteomics, vol. 73, no. 10, pp. 1907-1920, 2010.
13. L. E. Graves, E. V. Ariztia, J. R. Navari, H. J. Matzel, M. S. Stack, and D. A. Fishman, "Proinvasive properties of ovarian cancer ascites-derived membrane vesicles," Cancer Research, vol. 64, no. 19, pp. 7045-7049, 2004.
14. A. Piccin, W. G. Murphy, and O. P. Smith, "Circulating micro-particles: pathophysiology and clinical implications," Blood Reviews, vol. 21, no. 3, pp. 157-171, 2007.
15. D. M. Smalley, N. E. Sheman, K. Nelson, and D. Teodorescu, "Isolation and identifcation of potential urinary microparticle biomarkers of bladder cancer," Journal of Proteome Research, vol. 7, no. 5, pp. 2088-2096, 2008.
16. D. D. Taylor and C. Gercel-Taylor, "MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer," Gynecologic Oncology, vol. 110, no. 1, pp. 13-21, 2008.
17. H. Peinado, M. Alěcković, S. Lavotshkin et al., "Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET," Nature Medicine, vol. 18, no. 6, pp. 883-891, 2012.
18. H. Shao, J. Chung, L. Balaj et al., "Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy," Nature Medicine, vol. 18, no. 12, pp. 1835-1840, 2012.
19. Y. Yoshioka, N. Kosaka, Y. Konishi et al., "Ultra-sensitive liquid biopsy of circulating extracellular vesicles using ExoScreen," Nature Communications, vol. 5, article 3591, 2014.
20. H. Im, H. Shao, Y. I. Park et al., "Label-free detection and molecular profling of exosomes with a nano-plasmonic sensor," Nature Biotechnology, vol. 32, no. 5, pp. 490-495, 2014.
21. R. Jaenisch and A. Bird, "Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals," Nature Genetics, vol. 33, pp. 245-254, 2003.
22. Y. Lee, S. El Andaloussi, and M. J. A. Wood, "Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy," Human Molecular Genetics, vol. 21, no. 1, Article ID dds317, pp. R125-R134, 2012.
23. S. El Andaloussi, I. Mäger, X. O. Breakefeld, and M. J. A. Wood, "Extracellular vesicles: biology and emerging therapeutic opportunities," Nature Reviews Drug Discovery, vol. 12, no. 5, pp. 347-357, 2013.
24. A. Sharma, "Bioinformatic analysis revealing association of exosomal mRNAs and proteins in epigenetic inheritance," Journal of Teoretical Biology, vol. 357, pp. 143-149, 2014.
25. H. Valadi, K. Ekström, A. Bossios, M. Sjöstrand, J. J. Lee, and J. O. Lötvall, "Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells," Nature Cell Biology, vol. 9, no. 6, pp. 654-659, 2007.
26. G. Rabinowits, C. Gerçel-Taylor, J. M. Day, D. D. Taylor, and G. H. Kloecker, "Exosomal microRNA: a diagnostic marker for lung cancer," Clinical Lung Cancer, vol. 10, no. 1, pp. 42-46, 2009.
27. F. Chik, M. Szyf, and S. A. Rabbani, "Role of epigenetics in cancer initiation and progression," Advances in Experimental Medicine and Biology, vol. 720, pp. 91-104, 2011.
28. S. D. Fouse and J. F. Costello, "Epigenetics of neurological cancers," Future Oncology, vol. 5, no. 10, pp. 1615-1629, 2009.
29. O. Kovalchuk, V. P. Tryndyak, B. Montgomery et al., "Estrogen-induced rat breast carcinogenesis is characterized by alterations in DNA methylation, histone modifcations and aberrant microRNA expression," Cell Cycle, vol. 6, no. 16, pp. 2010-2018, 2007.
30. K. D. Robertson, E. Uzvolgyi, G. Liang et al., "The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors," Nucleic Acids Research, vol. 27, no. 11, pp. 2291-2298, 1999.
31. C. Popp, W. Dean, S. Feng et al., "Genome-wide erasure of DNA methylation in mouse primordial germ cells is afected by AID defciency," Nature, vol. 463, no. 7284, pp. 1101-1105, 2010.
32. L. Shen, H. Wu, D. Diep et al., "Genome-wide analysis reveals TET-and TDG-dependent 5-methylcytosine oxidation dynamics," Cell, vol. 153, no. 3, pp. 692-706, 2013.
33. J. Ratajczak, M. Wysoczynski, F. Hayek, A. Janowska-Wiec-zorek, and M. Z. Ratajczak, "Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication," Leukemia, vol. 20, no. 9, pp. 1487-1495, 2006.
34. X. Zhu, Y. You, Q. Li et al., "BCR-ABL1-positive microvesicles transform normal hematopoietic transplants through genomic instability: Implications for donor cell leukemia," Leukemia, vol. 28, no. 8, pp. 1666-1675, 2014.
35. Y. Yoshioka, Y. Konishi, N. Kosaka, T. Katsuda, T. Kato, and T. Ochiya, "Comparative marker analysis of extracellular vesicles in diferent human cancer types," Journal of Extracellular Vesicles, vol. 2, 2013.
36. C. Kahlert, S. A. Melo, A. Protopopov et al., "Identifcation of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer," The Journal of Biological Chemistry, vol. 289, no. 7, pp. 3869-3875, 2014.
37. Y. Yoshida, H. Yamamoto, R. Morita et al., "Detection of DNA methylation of gastric juice-derived exosomes in gastric cancer," Integrative Molecular Medicine, 2014.
38. Y. Watanabe, H. S. Kim, R. J. Castoro et al., "Sensitive and specifc detection of early gastric cancer with DNA methylation analysis of gastric washes," Gastroenterology, vol. 136, no. 7, pp. 2149-2158, 2009.
39. Y. Oishi, Y. Watanabe, Y. Yoshida et al., "Hypermethylation of Sox17 gene is useful as a molecular diagnostic application in early gastric cancer," Tum or Biology, vol. 33, no. 2, pp. 383-393, 2012.
40. D. Vigetti, M. Viola, E. Karousou et al., "Epigenetics in extracellular matrix remodeling and hyaluronan metabolism," FEBS Journal, vol. 281, no. 22, pp. 4980-4992, 2014.
41. S. U. Kass and A. P. Wolfe, "DNA methylation, nucleosomes and the inheritance of chromatin structure and function," Novartis Foundation Symposium, vol. 214, pp. 22-50, 1998.
42. M. Verma and S. Srivastava, "Epigenetics in cancer: implications for early detection and prevention," The Lancet Oncology, vol. 3, no. 12, pp. 755-763, 2002.
43. A. Munshi, G. Shaf, N. Aliya, and A. Jyothy, "Histone modif-cations dictate specifc biological readouts," Journal of Genetics and Genomics, vol. 36, no. 2, pp. 75-88, 2009.
44. K. K. Lee and J. L. Workman, "Histone acetyltransferase complexes: one size doesn't ft all," Nature Reviews Molecular Cell Biology, vol. 8, no. 4, pp. 284-295, 2007.
45. B. Li, M. Carey, and J. L. Workman, "The role of chromatin during transcription," Cell, vol. 128, no. 4, pp. 707-719, 2007.
46. H. Hou and H. Yu, "Structural insights into histone lysine demethylation," Current Opinion in Structural Biology, vol. 20, no. 6, pp. 739-748, 2010.
47. P. Gallinari, S. Di Marco, P. Jones, M. Pallaoro, and C. Steinkühler, "HDACs, histone deacetylation and gene transcription: from molecular biology to cancer therapeutics," Cell Research, vol. 17, no. 3, pp. 195-211, 2007.
48. M.-H. Kuo and C. D. Allis, "Roles of histone acetyltransferases and deacetylases in gene regulation," BioEssays, vol. 20, no. 8, pp. 615-626, 1998.
49. M. Grunstein, "Histone acetylation in chromatin structure and transcription," Nature, vol. 389, no. 6649, pp. 349-352, 1997.
50. A. Sharma, "Novel transcriptome data analysis implicates circulating microRNAs in epigenetic inheritance in mammals," Gene, vol. 538, no. 2, pp. 366-372, 2014.
51. S. Mathivanan, C. J. Fahner, G. E. Reid, and R. J. Simpson, "ExoCarta 2012: database of exosomal proteins, RNA and lipids," Nucleic Acids Research, vol. 40, no. 1, pp. D1241-D1244, 2012.
52. R. J. Simpson, H. Kalra, and S. Mathivanan, "ExoCarta as a resource for exosomal research," Journal of Extracellular Vesicles, vol. 1, Article ID 18374, 2012.
53. G. Schiera, C. M. Di Liegro, P. Saladino et al., "Oligoden-droglioma cells synthesize the diferentiation-specifc linker histone H1° and release it into the extracellular environment through shed vesicles," International Journal of Oncology, vol. 43, no. 6, pp. 1771-1776, 2013.
54. A. Izzo, K. Kamieniarz, and R. Schneider, "The histone H1 family: specifc members, specifc functions?" Biological Chemistry, vol. 389, no. 4, pp. 333-343, 2008.
55. W. F. Marzluf, P. Gongidi, K. R. Woods, J. Jin, and L. J. Maltais, "The human and mouse replication-dependent histone genes," Genomics, vol. 80, no. 5, pp. 487-498, 2002.
56. N. Happel and D. Doenecke, "Histone H1 and its isoforms: contribution to chromatin structure and function," Gene, vol. 431, no. 1-2, pp. 1-12, 2009.
57. A. Kowalski and J. Pałyga, "Linker histone subtypes and their allelic variants," Cell Biology International, vol. 36, no. 11, pp. 981-996, 2012.
58. J. Zlatanova and D. Doenecke, "Histone H1 zero: a major player in cell diferentiation?" The FASEB Journal, vol. 8, no. 15, pp. 1260-1268, 1994.
59. D. I. Gabrilovich, P. Cheng, Y. Fan et al., "H1 histone and diferentiation of dendritic cells. A molecular target for tumor-derived factors," Journal of Leukocyte Biology, vol. 72, no. 2, pp. 285-296, 2002.
60. C. H. Lawrie, S. Gal, H. M. Dunlop et al., "Detection of elevated levels of tumour-associated microRNAs in serum of patients with difuse large B-cell lymphoma," British Journal of Haematology, vol. 141, no. 5, pp. 672-675, 2008.
61. P. S. Mitchell, R. K. Parkin, E. M. Kroh et al., "Circulating microRNAs as stable blood-based markers for cancer detection," Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 30, pp. 10513-10518, 2008.
62. R. Ma, T. Jiang, and X. Kang, "Circulating microRNAs in cancer: origin, function and application," Journal of Experimental and Clinical Cancer Research, vol. 31, no. 1, article 38, 2012.
63. V. Ambros, "The functions of animal microRNAs," Nature, vol. 431, no. 7006, pp. 350-355, 2004.
64. D. P. Bartel, "MicroRNAs: genomics, biogenesis, mechanism, and function," Cell, vol. 116, no. 2, pp. 281-297, 2004.
65. X. Huang, T. Yuan, M. Tschannen et al., "Characterization of human plasma-derived exosomal RNAs by deep sequencing," BMC Genomics, vol. 14, no. 1, article 319, 2013.
66. D. M. Pegtel, K. Cosmopoulos, D. A. Torley-Lawson et al., "Functional delivery of viral miRNAs via exosomes," Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 14, pp. 6328-6333, 2010.
67. D. J. Gibbings, C. Ciaudo, M. Erhardt, and O. Voinnet, "Multi-vesicular bodies associate with components of miRNA efector complexes and modulate miRNA activity," Nature Cell Biology, vol. 11, no. 9, pp. 1143-1149, 2009.
68. N. Kosaka, H. Iguchi, Y. Yoshioka, F. Takeshita, Y. Matsuki, and T. Ochiya, "Secretory mechanisms and intercellular transfer of microRNAs in living cells," Journal of Biological Chemistry, vol. 285, no. 23, pp. 17442-17452, 2010.
69. A. Zomer, T. Vendrig, E. S. Hopmans, M. van Eijndhoven, J. M. Middeldorp, and D. M. Pegtel, "Exosomes: ft to deliver small RNA," Communicative & Integrative Biology, vol. 3, no. 5, pp. 447-450, 2014.
70. G. Rappa, J. Mercapide, F. Anzanello et al., "Wnt interaction and extracellular release of prominin-1/CD133 in human malignant melanoma cells," Experimental Cell Research, vol. 319, no. 6, pp. 810-819, 2013.
71. A. Lorico, J. Mercapide, and G. Rappa, "Prominin-1 (CD133) and metastatic melanoma: current knowledge and therapeutic perspectives," Advances in Experimental Medicine and Biology, vol. 777, pp. 197-211, 2013.
72. G. Rappa, O. Fodstad, and A. Lorico, "The stem cell-associated antigen CD133 (Prominin-1) is a molecular therapeutic target for metastatic melanoma," Stem Cells, vol. 26, no. 12, pp. 3008-3017, 2008.
73. G. Rappa, J. Mercapide, F. Anzanello, R. M. Pope, and A. Lorico, "Biochemical and biological characterization of exosomes containing prominin-1/CD133," Molecular Cancer, vol. 12, no. 1, article 62, 2013.
74. K. Ohshima, K. Inoue, A. Fujiwara et al., "Let-7 microRNA family Is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line," PLoS ONE, vol. 5, no. 10, Article ID e13247, 2010.
75. S. Rana, K. Malinowska, and M. Zöller, "Exosomal tumor microRNA modulates premetastatic organ cells," Neoplasia, vol. 15, no. 3, pp. 281-295, 2013.
76. C. Grange, M. Tapparo, F. Collino et al., "Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche," Cancer Research, vol. 71, no. 15, pp. 5346-5356, 2011.
77. S. Taverna, V. Amodeo, L. Saieva et al., "Exosomal shuttling of miR-126 in endothelial cells modulates adhesive and migratory abilities of chronic myelogenous leukemia cells," Molecular Cancer, vol. 13, no. 1, article 169, 2014.
78. N. Tominaga, N. Kosaka, M. Ono et al., "Brain metastatic cancer cells release microRNA-181c-containing extracellular vesicles capable of destructing blood-brain barrier," Nature Communications, vol. 6, p. 6716, 2015.
79. W. Zhou, M. Y. Fong, Y. Min et al., "Cancer-Secreted miR-105 destroys vascular endothelial barriers to promote metastasis," Cancer Cell, vol. 25, no. 4, pp. 501-515, 2014.
80. M. Ono, N. Kosaka, N. Tominaga et al., "Exosomes from bone marrow mesenchymal stem cells contain a microRNA that promotes dormancy in metastatic breast cancer cells," Science Signaling, vol. 7, no. 332, article ra63, 2014.
81. N. Kosaka, H. Iguchi, K. Hagiwara, Y. Yoshioka, F. Takeshita, and T. Ochiya, "Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic micrornas regulate cancer cell metastasis," The Journal of Biological Chemistry, vol. 288, no. 15, pp. 10849-10859, 2013.
82. T. Kogure, W.-L. Lin, I. K. Yan, C. Braconi, and T. Patel, "Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth," Hepatology, vol. 54, no. 4, pp. 1237-1248, 2011.
83. S.-I. Ohno, M. Takanashi, K. Sudo et al., "Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells," Molecular Terapy, vol. 21, no. 1, pp. 185-191, 2013.
84. J. M. Perkel, "Visiting 'noncodarnia'," BioTechniques, vol. 54, no. 6, pp. 301-304, 2013.
85. I. Grammatikakis, A. C. Panda, K. Abdelmohsen, and M. Gorospe, "Long noncoding RNAs (lncRNAs) and the molecular hallmarks of aging," Aging, vol. 6, no. 12, pp. 992-1009, 2014.
86. U. Gezer, E. Özgür, M. Cetinkaya, M. Isin, and N. Dalay, "Long non-coding RNAs with low expression levels in cells are enriched in secreted exosomes," Cell Biology International, vol. 38, no. 9, pp. 1076-1079, 2014.
87. T. Kogure, I. K. Yan, W.-L. Lin, and T. Patel, "Extracellular vesicle-mediated transfer of a novel long noncoding RNA TUC339: a mechanism of intercellular signaling in human hepatocellular cancer," Genes & Cancer, vol. 4, no. 7-8, pp. 261-272, 2013.
88. C. Braconi, N. Valeri, T. Kogure et al., "Expression and functional role of a transcribed noncoding RNA with an ultracon-served element in hepatocellular carcinoma," Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 2, pp. 786-791, 2011.
89. K. Takahashi, I. K. Yan, T. Kogure, H. Haga, and T. Patel, "Extracellular vesicle-mediated transfer of long non-coding RNA ROR modulates chemosensitivity in human hepatocellu-lar cancer," FEBS Open Bio, vol. 4, pp. 458-467, 2014.
90. L. H. Schmidt, T. Spieker, S. Koschmieder et al., "The long noncoding MALAT-1 RNA indicates a poor prognosis in non-small cell lung cancer and induces migration and tumor growth," Journal of Toracic Oncology, vol. 6, no. 12, pp. 1984-1992, 2011.
91. R. Lin, S. Maeda, C. Liu, M. Karin, and T. S. Edgington, "A large noncoding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomas," Oncogene, vol. 26, no. 6, pp. 851-858, 2007.
92. D. G. Weber, G. Johnen, S. Casjens et al., "Evaluation of long noncoding RNA MALAT1 as a candidate blood-based biomarker for the diagnosis of non-small cell lung cancer," BMC Research Notes, vol. 6, no. 1, article 518, 2013.
93. S. Raimondo, L. Saieva, C. Corrado et al., "Chronic myeloid leukemia-derived exosomes promote tumor growth through an autocrine mechanism," Cell Communication and Signaling, vol. 13, no. 1, article 8, 2015.
94. C. Corrado, S. Raimondo, A. Chiesi, F. Ciccia, G. De Leo, and R. Alessandro, "Exosomes as intercellular signaling organelles involved in health and disease: basic science and clinical applications," International Journal of Molecular Sciences, vol. 14, no. 3, pp. 5338-5366, 2013.